Efficacy of Respiratory Muscle Training in the Immediate Postoperative Period of Cardiac Surgery: A Systematic Review and Meta-Analysis

Introduction This study aimed to evaluate the efficacy of respiratory muscle training during the immediate postoperative period of cardiac surgery on respiratory muscle strength, pulmonary function, functional capacity, and length of hospital stay. Methods This is a systematic review and meta-analysis. A comprehensive search on PubMed®, Excerpta Medica Database (or Embase), Cumulative Index of Nursing and Allied Health Literature (or CINAHL), Latin American and Caribbean Health Sciences Literature (or LILACS), Scientific Electronic Library Online (or SciELO), Physiotherapy Evidence Database (or PEDro), and Cochrane Central Register of Controlled Trials databases was performed. A combination of free-text words and indexed terms referring to cardiac surgery, coronary artery bypass grafting, respiratory muscle training, and clinical trials was used. A total of 792 studies were identified; after careful selection, six studies were evaluated. Results The studies found significant improvement after inspiratory muscle training (IMT) (n = 165, 95% confidence interval [CI] 9.68, 21.99) and expiratory muscle training (EMT) (n = 135, 95% CI 8.59, 27.07) of maximal inspiratory pressure and maximal expiratory pressure, respectively. Also, IMT increased significantly (95% CI 19.59, 349.82, n = 85) the tidal volume. However, no differences were found in the peak expiratory flow, functional capacity, and length of hospital stay after EMT and IMT. Conclusion IMT and EMT demonstrated efficacy in improving respiratory muscle strength during the immediate postoperative period of cardiac surgery. There was no evidence indicating the efficacy of IMT for pulmonary function and length of hospital stay and the efficacy of EMT for functional capacity.


INTRODUCTION
Approximately 1.9 million people worldwide die each year from cardiovascular diseases (CVDs) [1] .In order to control these diseases, significant advances have been made in clinical practice for both diagnostic and treatment purposes [2] .Although conservative treatment may reduce CVD mortality rate, surgical treatment is necessary in many cases.Thereby, coronary artery bypass grafting (CABG) and valve replacement have been the gold standard treatments [2,3] .However, cardiac surgery may lead to several complications, mainly induced by sternotomy and extracorporeal circulation, such as respiratory muscle weakness, reduction in pulmonary function, and pulmonary infections, especially in the immediate postoperative period, which comprises the first hours after surgery until hospital discharge [4,5] .Furthermore, in order to avoid sternotomy-induced pain, patients maintain a shallow breathing pattern, which would restrict their chest movement, leading to a loss of respiratory muscle strength and diaphragm dysfunction [6] .Taken together, these cardiac surgery-induced changes increase the risk of mortality, length of stay, and patient costs [6] .In this scenario, the role of physiotherapy is extremely important.Physiotherapy includes a range of techniques, such as early mobilization, breathing exercises, coughing techniques, incentive spirometry, continuous positive airway pressure, and respiratory muscle training (RMT), in the preoperative and postoperative periods of cardiac surgery, in order to prevent complications [7,8] .Moreover, especially in the immediate postoperative period, this intervention is essential.
RMT is widely used and recognized among the physiotherapeutic approaches used during the pre and postoperative periods of cardiac surgery.It increases inspiratory and expiratory muscle strength, as well as preventing respiratory muscle weakness, and reducing respiratory complications [9,10] [9][10][11] .
Although several studies have demonstrated the importance of respiratory strength training after cardiac surgery, few studies have evaluated this treatment in the immediate postoperative period, and most of them used inspiratory strength training [12][13][14][15] .A metaanalysis had already shown the benefits of IMT (improvement of inspiratory muscle strength, pulmonary function, and functional capacity) before and after cardiac surgery [11] , however, without investigating the effect of expiratory strength training.In addition, to our knowledge, no study has evaluated the effect of RMT in the immediate postoperative period of cardiac surgery based on the overall quality of evidence of the Grading of Recommendations, Assessment, Development and Evaluation (GRADE) approach [16] , which offers a transparent structure for presenting evidence with recommendations for clinical practice.This systematic review and meta-analysis aimed to investigate and evaluate the effects of IMT and EMT on respiratory muscle strength, pulmonary function, functional capacity, and hospital stay in the immediate postoperative period of cardiac surgery in comparison to usual care, based on the quality of evidence by the GRADE approach.

Protocol and Registration
This meta-analysis was previously registered in the International Prospective Register of Systematic Reviews -PROSPERO (registration number CRD42018092593), following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (or PRISMA) guidelines [17] .

Eligibility Criteria
The present study included randomized controlled trials that evaluated the efficacy of EMT and/or IMT in patients after the immediate postoperative period of cardiac surgery, except heart transplantation, before hospital discharge.Studies that (I) performed RMT before cardiac surgery and (II) which the sample size was not provided by the authors were excluded.

Types of Interventions
The studies evaluated used mainly groups of patients undergoing inspiratory strength training, IMT, and EMT compared to groups of patients undergoing usual care.RMT was conducted using devices with inspiratory or expiratory loads, while the control group was represented by usual care, such as early mobilization, bronchial hygiene, breathing exercises without loads, and visits of nursing and medical staff.

Outcomes
The main outcomes considered in this review were respiratory muscle strength, evaluated by maximal inspiratory and expiratory pressures (cmH₂O); lung function, evaluated by tidal volume (mL) and expiratory peak flow (L/min); and functional capacity, evaluated by six-minute walk test (m) and length of hospital stay (days).All outcomes were analyzed within a period of up to 10 days of hospitalization since after that period, the patients had already been discharged from the hospital.

Electronic Search
In

Study Selection
The study selection was performed by two independent coauthors (T.N.A. and G.G.) in two phases to determine which articles were suitable.At first, duplicated and nonrelevant studies were discarded by examining titles and abstracts.Secondly, in accordance with the study inclusion and exclusion criteria, eligible studies were extracted by reviewing full-text articles.Any disagreements between the reviewers were resolved by consensus, and if necessary, a third reviewer (J.P.P.) was asked to decide on the inclusion of the studies.

Data Collection Process
The data relating to the number of participants and their characteristics (sex, age, and type of cardiac surgery) were extracted.
A description of the intervention and the comparisons, the outcome assessment tools, and the study results were also obtained.Lastly, for studies in which some data was not presented in the manuscript, we contacted the authors [18] , and the data were provided successfully.

Assessment of Methodological Quality of Studies
To assess the methodological quality of the studies, we use the PEDro scale [19] , which is an 11-item scale designed for rating methodological quality of clinical trials.Each satisfied item (except for item 1, which, unlike other scale items, pertains to external validity) contributes one point to the total PEDro scale (range = 0-10 points).The PEDro scores ranged from 4 to 10 -scores ranging from 9 to 10 were considered methodologically to be of "excellent" quality, scores from 6 to 8 were of "good" quality, scores 4 or 5 were of "fair" quality, and scores < 4 were felt to be of "poor" quality.Of all six studies evaluated using the PEDro scale, only one study was of "high quality" [18] .In addition to the PEDro score and according to the GRADE approach, when > 25% of the studies were of low quality, the assessment of the quality of the evidence was downgraded due to the risk of bias [16] .

Quality Assessment of the Evidence
The overall quality of the evidence of the studies was rated in accordance with the GRADE approach [16] .It consists of five items: (I) study limitations (risk of bias); (II) inconsistency of results (heterogeneity); (III) indirectness of evidence; (IV) imprecision of the effect estimates; and (V) reporting bias.The quality of the evidence was classified into four categories: high, moderate, low, and very low [20] .This approach entails the downgrading of evidence from high to moderate, to low, and to very low quality based on certain criteria.The criteria for downgrading the evidence one level were: (I) for study limitation, if the majority of studies (> 50%) was rated as high risk of bias; (II) for inconsistency, if heterogeneity was greater than the accepted low level (I 2 > 40%); (III) for indirectness, if the RMT session does not correspond to what is used in clinical practice; and (IV) for imprecision, if meta-analysis had small sample size (n < 300).

Statistical Analysis
All analyses were accomplished by random-effects models [21] .Median and standard deviation were used as summary statistics in meta-analysis once outcome measurements in all studies had the same scale [22] .In addition, the heterogeneity of results across the studies was evaluated using the I 2 statistic, interpreted as might not be important (0%-40%), may represent moderate (30%-60%), may represent substantial (50%-90%), and considerable (75%-100%) heterogeneity [22] .For meta-analysis, the Review Manager Software version 5.3 (RevMan, Copenhagen, Denmark) was used, which provides combined estimates with a 95% confidence interval (CI).

Study Selection
A total of 792 studies were identified in the literature search process to seek out systematic reviews with meta-analysis focused on this field.A consensus was reached and ended in a total of six potentially relevant studies, which were reviewed in full text, met the eligibility criteria, and were included in this review [12][13][14][15]23] (Figure 1). The tudies were published between 2009 and 2018, with a total of 298 participants.In addition, men had a higher frequency of CVDs (72%).
For IMT interventions, the IMT Respironics Threshold™ or the DHD IMT devices with a load equivalent to 40% of the maximal inspiratory pressure were used.When the intervention was EMT, the PEP Respironics Threshold™ and Respilift devices were used.The control groups were characterized by usual care, such as placebo treatment, nursing care, deep breathing, and early mobilization.

Methodological Quality of Studies
Five of the six studies had already identified the risk of bias from the PEDro database [12][13][14]18] . In acordance with the PEDro score, the mean for risk of bias of the six studies evaluated in this review was 4.6 (standard deviation = 1.75), which indicates that they are considered to be of fair quality (Table 2).

Comparison Between Inspiratory Muscle Training and Usual Care for Inspiratory Muscle Strength
Four included trials (n = 165) investigated the effect of IMT compared to usual care [12][13][14][15] .The pooled estimate showed that IMT improved inspiratory muscle strength by 15.83 cmH₂O (95% CI: 9.68-21.99,I 2 = 28%) (Figure 2A).According to the GRADE approach, the overall quality of evidence was rated as low quality (i.e., downgraded for the risk of bias, imprecision, and publication bias) (Table 3).

Comparison Between Inspiratory Muscle Training and Usual Care for Tidal Volume
The investigation of IMT compared to usual care for tidal volume after cardiac surgery was performed by two clinical trials (n = 85) [13,14] .
Brazilian Journal of Cardiovascular Surgery According to the pooled estimate, IMT improved the tidal volume by 184.7 mL (95% CI: 19.59-349.82,I 2 = 81%) (Figure 2B).The overall quality of evidence according to the GRADE approach was rated as very low quality (i.e., downgraded for inconsistency, imprecision, risk of bias, and publication bias) (Table 3).

Comparison Between Inspiratory Muscle Training and Usual Care for Expiratory Peak Flow
To compare the effect of IMT to the effect of usual care on expiratory peak flow, two trials were included (n = 85) [13,14] .There was no difference between the studies about expiratory peak flow by pooled estimate (95% CI: -14.93-107,I 2 = 54%) (Figure 2C).Thus, the overall quality of evidence was rated as very low quality (i.e., downgraded for inconsistency, imprecision, risk of bias, and publication bias), according to the GRADE approach (Table 3).

Comparison Between Inspiratory Muscle Training and Usual Care for the Length of Hospital Stay
Two included trials (n = 88) investigated the effect of IMT compared to usual care [13,15] .The pooled estimate showed that there was no CINAHL=Cumulative Index of Nursing and Allied Health Literature; Embase=Excerpta Medica Database; LILACS=Latin American and Caribbean Health Sciences Literature; PEDro=Physiotherapy Evidence Database; SciELO=Scientific Electronic Library Online.
difference between the studies about the length of hospital stay (95% CI: -3.69-2.58,I 2 = 91%) (Figure 2D).The overall quality of evidence according to the GRADE approach was rated as very low quality (i.e., downgraded for inconsistency, imprecision, risk of bias, and publication bias) (Table 3).

Comparison Between Expiratory Muscle Training and Minimal Interventions for Expiratory Muscle Strength
The effect of EMT compared to usual care was evaluated in two trials (n = 135) [18,23] .The pooled estimate showed that EMT improved expiratory muscle strength by 17.83 cmH₂O (95% CI: 78.59-27.07,I 2 = 0%) (Figure 3A).The overall quality of evidence according to the GRADE approach was rated as low quality (i.e., downgraded for the risk of bias, imprecision, and publication bias) (Table 4).

Comparison Between Expiratory Muscle Training and Minimal Interventions for Functional Capacity
Of the six trials, two (n = 135) investigated the effect of EMT compared to usual care for functional capacity [18,23] .The pooled estimate showed that there was no difference between the studies    ) and the small number of published studies c There are studies registered, but not published dBased on a small number of events, we consider reducing the of evidence, even with the seemingly narrow CI about functional capacity (12.74 meters) (95% CI: -18.81-44.29,I 2 = 0%) (Figure 3B).The overall quality of evidence according to the GRADE approach was rated as very low quality (i.e., downgraded for the risk of bias, inconsistency, imprecision, and publication bias) (Table 4).

Sensitivity Analysis
Regarding sensitivity analysis, four comparisons exhibited heterogeneity > 40%.The comparison of IMT and minimal interventions for tidal volume, expiratory peak flow, and length of hospital stay had I 2 values of 81%, 54%, and 91%, respectively.The comparison of EMT and usual care for functional capacity had an I 2 value of 69%.Performing a sensitivity analysis was not possible because of the low number (two) of studies for each comparison.These heterogeneities are related to the clinical heterogeneity of the studies with different types of interventions and outcomes.

DISCUSSION
RMT may significantly reduce complications induced by cardiac surgery.However, most studies are generally of low methodological quality, and they are highly heterogeneous with regard to the population, intervention, and measurement instruments investigated.
The current review meta-analysis focused on evaluating the effect of respiratory muscle strength training in the immediate postoperative period of cardiac surgery, especially in addition to strength, lung function, physical capacity, and length of hospital stay.Thus, the results demonstrated that the RMT improves both inspiratory and expiratory muscle strength [12][13][14][15]23] and tidal volume [13,14] . Furhermore, no difference was found after RMT on the variables peak expiratory flow [13,14] , length of hospital stay [13,15] , and functional capacity [18,23] .These authors suggest that the low impact of RMT on these outcomes may be due to the small sample size and the number of losses that occurred in some studies, in addition to the lack of comparison between pre and postoperative values. In addiion, there are still few clinical trials that have evaluated these outcomes, and future studies that do not present the previously described biases will be necessary to evaluate the effectiveness of the RMT on expiratory flow, length of hospital stay, and functional capacity.Thus, to our knowledge, this was the first study that evaluated the efficacy of IMT and EMT in the immediate postoperative period of cardiac surgery based on the general quality of evidence, through GRADE.
Based on the GRADE approach, we also found that during the immediate postoperative period of cardiac surgery, the RMT was superior to usual care.Furthermore, the GRADE evidence for these results demonstrated a low to very low quality, without significative differences between studies that evaluated expiratory peak flow and length of hospital stay.In addition, based on very low evidence and no statistical difference, the EMT did not alter functional capacity.However, the results demonstrated that this therapy may improve expiratory muscle strength.In addition, IMT may improve inspiratory muscle strength, however, it is uncertain whether this therapy may improve tidal volume, peak expiratory flow, and functional capacity in this population.Most of the clinical trials included in this review exhibited low methodological quality, according to PEDro [19] .This methodological analysis combined with GRADE [16] allows better evaluation and grading of evidence and greater confidence in the results of the Based on a small number of events, we consider reduction of evidence, even with the seemingly narrow CI c There are studies registered, but not published present study.A sensitive search strategy was used to identify the studies in the main databases.It was complemented by a manual search in the relevant studies and clinical trial registries.There were no language restrictions regarding the included studies, thus minimizing publication and language biases.However, it is possible that studies that were indexed only in local databases were missed and were consequently not included in this review.
Only three studies registered on clinical trial registration platforms were tracked.Since there is a risk of complications during the postoperative period of cardiac surgery, especially immediately after this procedure, the results of this review highlight the importance of respiratory strength training.As verified after this search, few studies have been developed evaluating expiratory strength training.Probably, since expiration is a passive mechanism which does not require as much force to be performed, studies have focused little on EMT.However, this fact does not justify not performing this exercise, since cardiac surgery reduces expiratory muscle strength, and maintaining it is essential for the good performance of lung function, as well as for maintaining ventilation and cough, which are essential for preventing infection, which may appear after surgery [19,24,25] .
In this review and meta-analysis, we demonstrated that EMT improves expiratory muscle strength, without present significative difference in the functional capacity, during the immediate postoperative period of cardiac surgery.However, only two trials used EMT for each outcome comparison.Additional studies should be carried out to better elucidate the effects of EMT immediately after cardiac surgery.Pulmonary complications after cardiac surgery are directly related to the length of hospital stay, that is, the longer the hospital stay, the greater the risk of developing complications [9] .In this context, two eligible studies in this meta-analysis evaluated the effect of the RMT on this outcome.The study conducted by Cordeiro et al. [15] demonstrated that IMT significantly reduced hospital stay days in patients undergoing CABG.And Barros et al. [13] did find a difference in the length of hospital stay after this intervention.IMT has been widely used in elective patients for cardiac surgery.However, most studies have investigated the effect of this intervention before cardiac surgery or after hospital discharge, during phases II or III of cardiac rehabilitation [9][10][11] .
Regarding IMT in the immediate postoperative period, our findings are similar to the ones of the review conducted by Gomes Neto et al. [11] .However, these authors did not associate EMT and did not use the GRADE approach to find a precise level of confidence in their results.Furthermore, they demonstrated an improvement of inspiratory muscle strength and pulmonary function, as well as a reduction of pulmonary complications, including trials performed up to June 2015, excluding recently published studies, which have been inserted in the present study.
The results of the present study indicate that IMT plays an important role in improving inspiratory muscle strength and tidal volume.
This finding shows the importance of RMT application in the acute postoperative period of cardiac surgery, which has reduced pulmonary function and inspiratory muscle strength, and consequently, complications.

Limitations
There are some limitations that should be considered in this study.Although the search was very comprehensive, few studies were eligible for the application of this meta-analysis.Thus, these factors reduced sample size, associated with low methodological quality and few similar outcomes for the comparisons.In addition, some sex-based inferences should be considered, since most studies were conducted with men.The age of patients was also not specified in most studies.Furthermore, sensitivity analyses stratified by methodological quality were also not possible.Thus, only a small number of studies have been examined.

CONCLUSION
In conclusion, this review demonstrated that both IMT and EMT demonstrated efficacy in improving respiratory muscle strength during the immediate postoperative period of cardiac surgery.
There was no evidence indicating the efficacy of IMT for pulmonary function and length of hospital stay and the efficacy of EMT for functional capacity.Thus, we suggest that future studies should be performed to help elucidate the benefits of RMT in the immediate perioperative period of cardiac surgery.
Financial support: This study was funded by the Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
No conflict of interest.

Fig. 1 -
Fig. 1 -Flowchart for trial selection according to Preferred Reporting Items for Systematic Reviews and Meta-analysis (or PRISMA).

3 *Fig. 2 -
Fig. 2 -Comparison between respiratory muscle training and usual care on respiratory muscle strength, pulmonary function, length of hospital stay, and functional capacity.CI=confidence interval; IMT=inspiratory muscle training; MIP=maximal inspiratory pressure; SD=standard deviation.

Fig. 3 -
Fig. 3 -Evidence level of respiratory muscle training on respiratory muscle strength, pulmonary function, length of hospital stay, and functional capacity.CI=confidence interval; EMT=expiratory muscle training; MEP=maximal expiratory pressure; SD=standard deviation.

Table 1 .
Overview of study design, participants, intervention, and results.

Study Participants Protocol used Results Male/female number Cardiac surgery type Average age ± SD and n. of patients per group Intervention Control
6MWT=six-minute walk test; CABG=coronary artery bypass grafting; CG=control group; EMS=expiratory muscle strength; EMT=expiratory muscle training; EPAP=expiratory positive airway pressure; EPF=expiratory peak flow; IG=intervention group; IMS=inspiratory muscle strength; IMT=inspiratory muscle training; MEP=maximal expiratory pressure; MIP=maximal inspiratory pressure; PEDro=Physiotherapy Evidence Database; PO3=third postoperative day; SD=standard deviation; TV=tidal volume; VC=vital capacity Period of Cardiac Surgery Braz J Cardiovasc Surg 2024;39(1):e20220165 Brazilian Journal of Cardiovascular Surgery

Table 2 .
Methodological quality of studies using the Physiotherapy Evidence Database (PEDro) score.

Table 3 .
Evidence of inspiratory muscle training compared to control (usual care) for inspiratory muscle strength, pulmonary function, and length of hospital stay.
a All studies presented a PEDro score of 4 out of 10 b Based on statistical criteria (I 2

Table 4 .
Evidence of expiratory muscle training compared to control group (minimal interventions) for expiratory muscle strength and functional capacity.